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Social and Genetic Structure of a Supercolonial Weaver Ant, Polyrhachis Robsoni, with Dimorphic Queens

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Social and Genetic Structure of a Supercolonial Weaver Ant, Polyrhachis Robsoni, with Dimorphic Queens Insect. Soc. 54 (2007) 34 – 41 0020-1812/07/010034-8 Insectes Sociaux DOI 10.1007/s00040-007-0909-x Birkhuser Verlag, Basel, 2007 Research article Social and genetic structure of a supercolonial weaver ant, Polyrhachis robsoni, with dimorphic queens J.S. van Zweden1,2, M.E. Carew3,4, M.T. Henshaw1,5, S.K.A. Robson1 and R.H. Crozier1,3,* 1 School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4810, Australia, e-mails: [email protected], [email protected] 2 Present address: Department of Population Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark, e-mail: [email protected] 3 School of Biochemistry, Chemistry and Genetics, La Trobe University, Bundoora, Victoria, Australia 4 Present address: CESAR, University of Melbourne, Parkville, Victoria 3052, Australia, e-mail: [email protected] 5 Present address: McKendree College, 701 College Road, Lebanon, Illinois 62254, USA, e-mail: [email protected] Received 19 July 2006; revised 16 October 2006; accepted 25 October 2006. Published Online First 19 January 2007 Abstract. We studied a population of the Australian Introduction weaver ant Polyrachis robsoni with regard to variation in the morphology of its winged queens using six newly- Morphological polymorphism between queens is wide- developed microsatellite markers. Morphometrically the spread in ants, with cases in at least seven subfamilies queens fell clearly into two groups, macrogynes and (Heinze and Keller, 2000). These cases range from simple microgynes, with the latter an isometric reduction of the size differences to both winged and wingless queens being former. Aggression tests showed that hostility between found in the same species. The interest in the cases of ants from different nests was minimal. Nests frequently simple size polymorphism stems from the fact that these contained numbers of both queen types, with microgynes may represent the initial stages of the process leading to about twice as numerous as macrogynes. Nestmate work- the winged/wingless dichotomy, to the presence of only ers, microgynes, and macrogynes, were significantly wingless queens if the winged ones are lost, or possibly to related to others within their caste, with macrogynes sympatric speciation. Typically, the smaller queens (mi- more highly related than the other castes. Relatedness crogynes) are isometric reductions of the larger queens values between these groups of nestmates were also (macrogynes), and together the two forms display a significant. Pairwise relatedness values were consistent bimodal frequency distribution of body size. Microgynes with both queen morphs producing workers. At the also typically have a reduced number of functional population level, microgynes from different nests were ovarioles compared to macrogynes, as well as reduced also significantly related and there was a weak inverse wings (Lachaud et al., 1999; Rüppell et al., 2001a), relationship between pairwise relatedness value between although there are cases where the number of ovarioles is individuals and distance between nests. We conclude that the same between the two queen forms (Rppell et al., this species is supercolonial and that the two queen 1998). morphs are part of the same population. Explanations for the presence of dimorphic queens vary, in part because of the highly-variable life history Keywords: Polyrhachis weaver ants, microsatellites, di- stategies of the species in which they have been found. morphic queens, dispersal, relatedness, supercolonies. The presence and number of macrogynes and microgynes within individual colonies or populations has been variously described as reflecting a variety of colony founding strategies, genetic polymorphism, or frequency dependent selection, but it has been difficult to derive common overall patterns and explanations (Heinze and Keller, 2000). For example, microgyne numbers are * Corresponding author greatest in larger colonies of Ectatomma ruidum (La- Insect. Soc. Vol. 54, 2007 Research article 35 chaud et al., 1999) and of Temnothorax rugatulus Methods (Rppell et al., 2001c). The general perception is that the larger size of Collection site and colony structure macrogynes reflects independent colony foundation producing monogynous nests, and the smaller microgynes We collected all 37 nests visible in a group of trees bordering the edges tend towards dependent colony foundation and are often of a small pond in the Botanical Gardens of Cairns, North Queensland, Australia (16830’’’S,145830’’’E). The pond runs SW to NE and is about associated with polygyny and limited gyne dispersal 100m wide; the collections were made on the NW and SE sides of the (Rppell and Heinze, 1999). The extent to which micro- terminus of the pond. The relative position of each nest was recorded, gynes act as intraspecific parasites and are adopted into along with the number of brood, workers and queens found in each nest. unrelated nests, or are adopted back into their natal To determine if different nests might belong to the same colonies, we conducted a series of laboratory based aggression tests as a bioassay colonies, remains unknown in most cases. But using for colony membership. A single individual from each of two test molecular markers to estimate relatedness between the colonies were placed in a circular observation chamber (diame- two queen types, Rppell and coworkers (2001b; 2003) ter=10 cm) and their first contact recorded on a aggression scale found for Temnothorax rugatulus that macrogynes pre- ranging from 0 to 4 (0=trophallaxis, 1=antennation, 2=touch without further interaction, 3=touch and avoidance, and 4=grabbing). This dominantly found colonies independently but micro- approach was replicated for a total of ten pairs of individuals from each gynes rejoin their natal nests. Although the same general pair of colonies tested and the average aggression scores used as a pattern is believed to occur in Temnothorax cf. andrei, measure of between-colony aggression. A total of 24 colonies (12 pairs queen morphology was not correlated with colony social of two) were selected from a variety of locations to provide a range of structure and a high rate of macrogynes rejoining natal between-colony distances, and individual colonies were only tested in one pair-wise comparison. colonies was suggested (Rppell et al., 2001a). The ant genus Polyrhachis is a taxonomically, ecolog- ically and socially diverse group. With over 450 species Queen morphology divided into 12 subgenera (Bolton, 1995; Dorow, 1995), nesting habits range from subterranean in either terres- For each individual queen we determined head length (from the posterior most point along the posterior occipital border to the anterior trial or intertidal habitats (Nielsen, 1997), to lignicolous, most point on the anterior clypeal border), head width (the distance lithophilic, and arboreal (Liefke et al., 1998; Robson, between the occipital lobes), mesosoma length (the first three 2004), with nests constructed of various combinations of postcephalic segments plus the propodeum, in side view) and meso- carton, larval and spider silk (Robson and Kohout, 2005). soma width (the distance between the two wing scars). Measurements were made using NIH Image 1.61 (National Institute of Health, USA) Colony structure can be highly variable, with some and images captured with a JVC digital video camera and a Leica MZ6 species establishing nests through either single or multi- binocular microscope. All measurements were taken three times from ple queens (Sasaki et al., 2005; Yamauchi et al., 1987) or each individual and the average was used in the analysis. obligatory parasitic relationships with other species of ants (Maschwitz et al., 2003). The Australian weaver ant Genetic analyses Polyrhachis robsoni (previously referred to as P. doddi? (Bellas and Hçlldobler, 1985), P. cf. doddi (Heinze and Microsatellites were isolated using methods described previously Hçlldobler, 1993), P. Cyrto 04 or P. Cyrto 05 (Kohout, (Crozier et al., 1999). 2000)) is a polydomous arboreal ant that constructs nests We used the microsatellite loci Prob5, Prob37, Prob90, Prob114, from the silk of its larvae (Kohout, 2006). Individual nests Prob130, and Prob220 to estimate relatedness values. All queens and at least six workers from each nest were analysed, to determine a measure can contain numerous dimorphic queens, each of which of allele frequencies of each nest and the population as a whole. has a full set of thoracic sclerites and seemingly functional DNA was extracted using a standard salt precipitation protocol wings. Both queen morphs appear capable of reproduc- (Miller et al., 1988; Strassmann et al., 1996). Briefly, we ground tion, possessing apparently functional ovaries, and to- individual thoraxes in 500 ml of grinding buffer (0.1M NaCl, 0.1M Tris- HCl (pH 9.1), 0.05M EDTA, 0.05% SDS) using a mini-pestle. Samples gether present a typical bimodal but continuous size were then incubated for 30 minutes in a 658C water bath, 86 mlof8M frequency distribution (Heinze and Hçlldobler, 1993). potassium acetate was then added and the mixture stored for 30–40 However, the sample sizes available to Heinze and minutes in 48C, to let salts and other minerals precipitate. The mixture Hçlldobler (1993) were relatively small and the actual was then centrifuged at 13000 rpm for 5 minutes, 400 ml of the reproductive output of individual queens was not deter- supernatant transferred to a new tube and combined with 1000 mlof À208C 100% High Grade Ethanol, and stored at À208C for at least 3 mined. In this study we use molecular markers for the first hours for the DNA to precipitate. Samples were then centrifuged at time for this species to infer relatedness patterns between 13000 rpm for 5 minutes, the ethanol poured off and the remaining macrogynes, microgynes and workers, examine the rela- pellet dried for 10 minutes in a Speed Vac. The DNA was re-suspended tionship between internest relatedness values and geo- in 50 ml of ultrapure ddH2O and then diluted six times for use in PCR. For PCR we used 96 well plates with a reaction volume of 10 mlin graphic distance, and clarify the queen size distribution.
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